On the evolution of heightened condition dependence of male sexual displays

The maintenance of genetic variation in male sexual display traits in the face of strong directional sexual selection from female preferences is an ongoing evolutionary conundrum. Condition dependence and the genic capture hypothesis are often cited as theoretical resolutions to this problem, yet little is known about the ability of condition dependence itself to evolve. We set out to test how a suite of cuticular hydrocarbons (CHCs) used in sexual displays are affected by adult diet and the potential for any condition-dependent response to evolve in a laboratory-adapted population of the Australian fruit fly Drosophila serrata. We performed a dietary manipulation within a half-sib breeding design, raising adult males either with or without access to live yeast, a manipulation that had previously shown strong effects on female fitness. Diet had strong phenotypic effects, with males from the different diets producing different CHC blends. The blend of CHCs under sexual selection showed a degree of elevated condition dependence. Regardless of the heightened sensitivity of favoured CHC blends to diet and the presence of genetic variance for the traits, we were unable to detect any genetic variance in the reaction norms for the male dietary response. Our results suggest that there is limited opportunity for males to evolve further condition dependence in response to yeast availability in this population.     

Gene or environment? Species-specific control of stomatal density and length

Stomatal characteristics are used as proxies of paleo-environment. Only a few model species have been used to study the mechanisms of genetic and environmental effects on stomatal initiation. Variation among species has not been quantified. In this paper, results from an in situ reciprocal transplant experiment along an elevation gradient in the northeast Tibetan Plateau are reported, in which the relative effects of genetics (original altitude) and environment (transplant altitude) on stomatal density (SD) and length (SL) were quantified. In Thalictrum alpinum, only the environment significantly influenced SD, with the variance component ([Formula: see text]) of the environment found to be much greater than that of genetics ([Formula: see text]) ([Formula: see text]). In Kobresia humillis, only genetics significantly influenced SD and SL, with the genetics variance component found to be greater than that of the environment ([Formula: see text], for SD). These results suggest that the extent to which genetics and the environment determine stomatal initiation and development is species-specific. This needs to be considered when studying genetic or environmental controls of stomatal initiation, as well as when SD and SL are used as proxies for ancient climate factors (e.g., CO(2) concentration).     

Robustness and information propagation in attractors of random boolean networks

Attractors represent the long-term behaviors of Random Boolean Networks. We study how the amount of information propagated between the nodes when on an attractor, as quantified by the average pairwise mutual information ([Formula: see text]), relates to the robustness of the attractor to perturbations ([Formula: see text]). We find that the dynamical regime of the network affects the relationship between [Formula: see text] and [Formula: see text]. In the ordered and chaotic regimes, [Formula: see text] is anti-correlated with [Formula: see text], implying that attractors that are highly robust to perturbations have necessarily limited information propagation. Between order and chaos (for so-called "critical" networks) these quantities are uncorrelated. Finite size effects cause this behavior to be visible for a range of networks, from having a sensitivity of 1 to the point where [Formula: see text] is maximized. In this region, the two quantities are weakly correlated and attractors can be almost arbitrarily robust to perturbations without restricting the propagation of information in the network.     

The depletion of genetic variance by sexual selection

Sexually selected traits display substantial genetic variance [1, 2], in conflict with the expectation that sexual selection will deplete it [3-5]. Condition dependence is thought to resolve this paradox [5-7], but experimental tests that relate the direction of sexual selection to the availability of genetic variance are lacking. Here, we show that condition-dependent expression is not sufficient to maintain genetic variance available to sexual selection in multiple male sexually selected traits. We employed an experimental design that simultaneously determined the quantitative genetic basis of nine male cuticular hydrocarbons (CHCs) of Drosophila bunnanda, the extent of condition dependence of these traits, and the strength and direction of sexual selection acting upon them. The CHCs of D. bunnanda are condition dependent, with 18% of the genetic variance in male body size explained by genetic variance in CHCs. Despite the presence of genetic variance in individual male traits, 98% of the genetic variance in CHCs was found to be orientated more than 88 degrees away from the direction of sexual selection and therefore unavailable to selection. A lack of genetic variance in male traits in the direction of sexual selection may represent a general feature of sexually selected systems, even in the presence of condition-dependent trait expression.     

Fracture Faces in the Cell Envelope of Escherichia coli

Freeze-fracturing of Escherichia coli cells in the presence of 30% (v/v) glycerol resulted in a double cleavage of the cell envelope exposing two convex and two concave fracture faces ([Formula: see text], [Formula: see text] and [Formula: see text], [Formula: see text]) with characteristic patterns. Complementary replicas revealed the relationship of the fracture faces to their corresponding fracture planes. The inner fracture plane splits the plasma membrane at one particular level. Apparently the outer fracture plane was located in the outer part of the wall, as it was separated by a layer ([Formula: see text]) from the fractured profile (CW1) presumably corresponding to the murein layer. The outer fracture plane did alternate toward the cell periphery, exposing complementary smooth areas ([Formula: see text] and [Formula: see text]). When cells were freeze-fractured in the absence of glycerol, the outer cell surface appeared as an etching face rather than a fracture face. A schematic representation of the relative location of the different fracture faces in the E. coli cell envelope is given.     

Sex-specific genotype-by-environment interactions for cuticular hydrocarbon expression in decorated crickets, Gryllodes sigillatus: implications for the evolution of signal reliability

Phenotypic traits that convey information about individual identity or quality are important in animal social interactions, and the degree to which such traits are influenced by environmental variation can have profound effects on the reliability of these cues. Using inbred genetic lines of the decorated cricket, Gryllodes sigillatus, we manipulated diet quality to test how the cuticular hydrocarbon (CHC) profiles of males and females respond across two different nutritional rearing environments. There were significant differences between lines in the CHC profiles of females, but the effect of diet was not quite statistically significant. There was no significant genotype-by-environment interaction (GEI), suggesting that environmental effects on phenotypic variation in female CHCs are independent of genotype. There was, however, a significant effect of GEI for males, with changes in both signal quantity and content, suggesting that environmental effects on phenotypic expression of male CHCs are dependent on genotype. The differential response of male and female CHC expression to variation in the nutritional environment suggests that these chemical cues may be under sex-specific selection for signal reliability. Female CHCs show the characteristics of reliable cues of identity: high genetic variability, low condition dependence and a high degree of genetic determination. This supports earlier work showing that female CHCs are used in self-recognition to identify previous mates and facilitate polyandry. In contrast, male CHCs show the characteristics of reliable cues of quality: condition dependence and a relatively higher degree of environmental determination. This suggests that male CHCs are likely to function as cues of underlying quality during mate choice and/or male dominance interactions.     

Beauty or function? The opposing effects of natural and sexual selection on cuticular hydrocarbons in male black field crickets

Although many theoretical models of male sexual trait evolution assume that sexual selection is countered by natural selection, direct empirical tests of this assumption are relatively uncommon. Cuticular hydrocarbons (CHCs) are known to play an important role not only in restricting evaporative water loss but also in sexual signalling in most terrestrial arthropods. Insects adjusting their CHC layer for optimal desiccation resistance is often thought to come at the expense of successful sexual attraction, suggesting that natural and sexual selection are in opposition for this trait. In this study, we sampled the CHCs of male black field crickets (Teleogryllus commodus) using solid-phase microextraction and then either measured their evaporative water loss or mating success. We then used multivariate selection analysis to quantify the strength and form of natural and sexual selection targeting male CHCs. Both natural and sexual selection imposed significant linear and stabilizing selection on male CHCs, although for very different combinations. Natural selection largely favoured an increase in the total abundance of CHCs, especially those with a longer chain length. In contrast, mating success peaked at a lower total abundance of CHCs and declined as CHC abundance increased. However, mating success did improve with an increase in a number of specific CHC components that also increased evaporative water loss. Importantly, this resulted in the combination of male CHCs favoured by natural selection and sexual selection being strongly opposing. Our findings suggest that the balance between natural and sexual selection is likely to play an important role in the evolution of male CHCs in T. commodus and may help explain why CHCs are so divergent across populations and species.     

Limits to the rate of adaptive substitution in sexual populations

In large populations, many beneficial mutations may be simultaneously available and may compete with one another, slowing adaptation. By finding the probability of fixation of a favorable allele in a simple model of a haploid sexual population, we find limits to the rate of adaptive substitution, [Formula: see text], that depend on simple parameter combinations. When variance in fitness is low and linkage is loose, the baseline rate of substitution is [Formula: see text], where [Formula: see text] is the population size, [Formula: see text] is the rate of beneficial mutations per genome, and [Formula: see text] is their mean selective advantage. Heritable variance [Formula: see text] in log fitness due to unlinked loci reduces [Formula: see text] by [Formula: see text] under polygamy and [Formula: see text] under monogamy. With a linear genetic map of length [Formula: see text] Morgans, interference is yet stronger. We use a scaling argument to show that the density of adaptive substitutions depends on [Formula: see text], [Formula: see text], [Formula: see text], and [Formula: see text] only through the baseline density: [Formula: see text]. Under the approximation that the interference due to different sweeps adds up, we show that [Formula: see text], implying that interference prevents the rate of adaptive substitution from exceeding one per centimorgan per 200 generations. Simulations and numerical calculations confirm the scaling argument and confirm the additive approximation for [Formula: see text]; for higher [Formula: see text], the rate of adaptation grows above [Formula: see text], but only very slowly. We also consider the effect of sweeps on neutral diversity and show that, while even occasional sweeps can greatly reduce neutral diversity, this effect saturates as sweeps become more common-diversity can be maintained even in populations experiencing very strong interference. Our results indicate that for some organisms the rate of adaptive substitution may be primarily recombination-limited, depending only weakly on the mutation supply and the strength of selection.     

Female choice for male cuticular hydrocarbon profile in decorated crickets is not based on similarity to their own profile

Indirect genetic benefits derived from female mate choice comprise additive (good genes) and nonadditive genetic benefits (genetic compatibility). Although good genes can be revealed by condition‐dependent display traits, the mechanism by which compatibility alleles are detected is unclear because evaluation of the genetic similarity of a prospective mate requires the female to assess the genotype of the male and compare it to her own. Cuticular hydrocarbons (CHCs), lipids coating the exoskeleton of most insects, influence female mate choice in a number of species and offer a way for females to assess genetic similarity of prospective mates. Here, we determine whether female mate choice in decorated crickets is based on male CHCs and whether it is influenced by females' own CHC profiles. We used multivariate selection analysis to estimate the strength and form of selection acting on male CHCs through female mate choice, and employed different measures of multivariate dissimilarity to determine whether a female's preference for male CHCs is based on similarity to her own CHC profile. Female mating preferences were significantly influenced by CHC profiles of males. Male CHC attractiveness was not, however, contingent on the CHC profile of the choosing female, as certain male CHC phenotypes were equally attractive to most females, evidenced by significant linear and stabilizing selection gradients. These results suggest that additive genetic benefits, rather than nonadditive genetic benefits, accrue to female mate choice, in support of earlier work showing that CHC expression of males, but not females, is condition dependent.     

The genetics of cuticular hydrocarbon profiles in the Fruit Fly Drosophila simulans

Female mate choice is one mechanism of sexual selection and, provided there is adequate genetic variation in the male traits that are the target of this selection, they will evolve via female choice. Cuticular hydrocarbons (CHCs) are important in Drosophila mate choice, but relatively little is known about the underlying genetic architecture of CHC profiles in Drosophila simulans. Here, we used gas chromatography-mass spectrometry to investigate patterns of genetic variation in the CHC profiles of male and female D. simulans using isofemale lines. We found substantial genetic variation for CHC profiles and individual CHC components, and individual CHCs were frequently strongly genetically correlated, with a tendency for negative covariance between long- and short-chain CHCs in males. Intersexual genetic covariances were often weak and frequently differed in sign. These findings are novel and significant, highlighting the previously unexplored genetic architecture of CHCs in D. simulans and suggest that this architecture may facilitate sex-specific CHC evolution.     

Reduced set of virulence genes allows high accuracy prediction of bacterial pathogenicity in humans

Although there have been great advances in understanding bacterial pathogenesis, there is still a lack of integrative information about what makes a bacterium a human pathogen. The advent of high-throughput sequencing technologies has dramatically increased the amount of completed bacterial genomes, for both known human pathogenic and non-pathogenic strains; this information is now available to investigate genetic features that determine pathogenic phenotypes in bacteria. In this work we determined presence/absence patterns of [Formula: see text] different virulence-related genes among more than [Formula: see text] finished bacterial genomes from both human pathogenic and non-pathogenic strains, belonging to different taxonomic groups (i.e: Actinobacteria, Gammaproteobacteria, Firmicutes, etc.). An accuracy of 95% using a cross-fold validation scheme with in-fold feature selection is obtained when classifying human pathogens and non-pathogens. A reduced subset of highly informative genes ([Formula: see text]) is presented and applied to an external validation set. The statistical model was implemented in the BacFier v1.0 software (freely available at [Formula: see text]), that displays not only the prediction (pathogen/non-pathogen) and an associated probability for pathogenicity, but also the presence/absence vector for the analyzed genes, so it is possible to decipher the subset of virulence genes responsible for the classification on the analyzed genome. Furthermore, we discuss the biological relevance for bacterial pathogenesis of the core set of genes, corresponding to eight functional categories, all with evident and documented association with the phenotypes of interest. Also, we analyze which functional categories of virulence genes were more distinctive for pathogenicity in each taxonomic group, which seems to be a completely new kind of information and could lead to important evolutionary conclusions.     

Experimental evidence for the role of sexual selection in the evolution of cuticular hydrocarbons in the dung beetle,Onthophagus taurus

A role for sexual selection in the evolution of insect cuticular hydrocarbons (CHCs) is suggested by observations of selection acting on male CHCs during female mate choice. However, evidence that CHCs evolve in response to sexual selection is generally lacking, and there is a need to extend our understanding beyond well‐studied taxa. Experimental evolution offers a powerful approach to investigate the effect of sexual selection on the evolution of insect CHCs. We conducted such an experiment using the dung beetle, Onthophagus taurus. After six, 12 and 21 generations of experimental evolution, we measured the CHCs of beetles from three populations subject to sexual selection and three populations within which sexual selection had been removed via enforced monogamy. We found that the male CHC profile responded to the experimental removal of sexual selection. Conversely, the CHC profile of females responded to the presence of sexual selection but not to its removal. These results show that sexual selection can be an important mechanism affecting the evolution of insect CHCs and that male and female CHCs can evolve independently.     

Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field-reared males and their laboratory-reared offspring allowed the estimation of the genetic variance-covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition-dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.     

Environmental heterogeneity,multivariate sexual selection and genetic constraints on cuticular hydrocarbons in Drosophila simulans

Sexual selection is responsible for the evolution of many elaborate traits, but sexual trait evolution could be influenced by opposing natural selection as well as genetic constraints. As such, the evolution of sexual traits could depend heavily on the environment if trait expression and attractiveness vary between environments. Here, male Drosophila simulans were reared across a range of diets and temperatures, and we examined differences between these environments in terms of (i) the expression of male cuticular hydrocarbons (CHCs) and (ii) which male CHC profiles were most attractive to females. Temperature had a strong effect on male CHC expression, whereas the effect of diet was weaker. Male CHCs were subject to complex patterns of directional, quadratic and correlational sexual selection, and we found differences between environments in the combination of male CHCs that were most attractive to females, with clearer differences between diets than between temperatures. We also show that genetic covariance between environments is likely to cause a constraint on independent CHC evolution between environments. Our results demonstrate that even across the narrow range of environmental variation studied here, predicting the outcome of sexual selection can be extremely complicated, suggesting that studies ignoring multiple traits or environments may provide an over‐simplified view of the evolution of sexual traits.     

Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata

The nature of male mating preferences, and how they differ from female mating preferences in species with conventional sex roles, has received little attention in sexual selection studies. We estimated the form and strength of sexual selection as a consequence of male and female mating preferences in a laboratory-based population of Drosophila serrata. The differences between sexual selection on male and female signal traits (cuticular hydrocarbons [CHCs]) were evaluated within a formal framework of linear and nonlinear selection gradients. Females tended to exert linear sexual selection on male CHCs, whereas males preferred intermediate female CHC phenotypes leading to convex (stabilizing) selection gradients. Possible mechanisms determining the nonlinear nature of sexual selection on female CHCs are proposed.     

Phenotypic selection on a heritable size trait revisited

One of evolutionary biology's most persistent puzzles is the fact that apparent directional selection on a heritable trait in a natural population often does not produce a selection response. We tested three possible explanations for this problem using data on body size of more than 23,000 individuals, measured over 18 yr, in a collared flycatcher (Ficedula albicollis) population. Using a restricted maximum likelihood "animal model," we found a narrow-sense heritability for fledgling tarsus length of [Formula: see text] SE and substantial common environment effects ([Formula: see text] SE). For survival to adulthood, the selection differential on tarsus length was [Formula: see text] SE. There was, however, no response to this selection over the study period. One explanation for the lack of response might have been that selection was associated with only the environmental (nonheritable) component of phenotype, but we found significant selection on breeding values (the heritable component). There was also no evidence of fluctuating selection pressures or of antagonistic selection between the sexes in selection pressures. Thus, in contrast to earlier investigations in this same population, none of the potential explanations for the absence of a selection response was supported; we discuss alternative hypotheses yet to be investigated.     

An evolutionary limit to male mating success

The well-known phenotypic diversity of male sexual displays, and the high levels of genetic variation reported for individual display traits have generated the expectation that male display traits, and consequently male mating success, are highly evolvable. It has not been shown however that selection for male mating success, exerted by female preferences in an unmanipulated population, results in evolutionary change. Here, we tested the expectation that male mating success is highly evolvable in Drosophila bunnanda using an experimental evolution approach. Female D. bunnanda exhibit a strong, consistent preference for a specific combination of male cuticular hydrocarbons (CHCs). We used female preference to select for male mating success by propagating replicate populations from either attractive or unattractive males over 10 generations. Neither the combination of CHCs under sexual selection (the sexual signal) nor male mating success itself evolved. The lack of a response to selection was consistent with previous quantitative genetic experiments in D. bunnanda that demonstrated the virtual absence of genetic variance in the combination of CHCs under sexual selection. Persistent directional selection, such as applied by female mate choice, may erode genetic variance, resulting in multitrait evolutionary limits.     

Genetic divergence and phenotypic plasticity contribute to variation in cuticular hydrocarbons in the seaweed fly Coelopa frigida

Cuticular hydrocarbons (CHCs) form the boundary between insects and their environments and often act as essential cues for species, mate, and kin recognition. This complex polygenic trait can be highly variable both among and within species, but the causes of this variation, especially the genetic basis, are largely unknown. In this study, we investigated phenotypic and genetic variation of CHCs in the seaweed fly, Coelopa frigida, and found that composition was affected by both genetic (sex and population) and environmental (larval diet) factors. We subsequently conducted behavioral trials that show CHCs are likely used as a sexual signal. We identified general shifts in CHC chemistry as well as individual compounds and found that the methylated compounds, mean chain length, proportion of alkenes, and normalized total CHCs differed between sexes and populations. We combined these data with whole genome resequencing data to examine the genetic underpinnings of these differences. We identified 11 genes related to CHC synthesis and found population‐level outlier SNPs in 5 that are concordant with phenotypic differences. Together these results reveal that the CHC composition of C. frigida is dynamic, strongly affected by the larval environment, and likely under natural and sexual selection.     

Differential effects of genetic vs. environmental quality in Drosophila melanogaster suggest multiple forms of condition dependence

Condition is a central concept in evolutionary ecology, but the roles of genetic and environmental quality in condition‐dependent trait expression remain poorly understood. Theory suggests that condition integrates genetic, epigenetic and somatic factors, and therefore predicts alignment between the phenotypic effects of genetic and environmental quality. To test this key prediction, we manipulated both genetic (mutational) and environmental (dietary) quality in Drosophila melanogaster and examined responses in morphological and chemical (cuticular hydrocarbon, CHC) traits in both sexes. While the phenotypic effects of diet were consistent among genotypes, effects of mutation load varied in magnitude and direction. Average effects of diet and mutation were aligned for most morphological traits, but non‐aligned for the male sexcombs and CHCs in both sexes. Our results suggest the existence of distinct forms of condition dependence, one integrating both genetic and environmental effects and the other purely environmental. We propose a model to account for these observations.     

Sexual Selection on male cuticular hydrocarbons via male–male competition and female choice

Traditional views of sexual selection assumed that male–male competition and female mate choice work in harmony, selecting upon the same traits in the same direction. However, we now know that this is not always the case and that these two mechanisms often impose conflicting selection on male sexual traits. Cuticular hydrocarbons (CHCs) have been shown to be linked to both social dominance and male attractiveness in several insect species. However, although several studies have estimated the strength and form of sexual selection imposed on male CHCs by female mate choice, none have established whether these chemical traits are also subject to sexual selection via male–male competition. Using a multivariate selection analysis, we estimate and compare sexual selection exerted by male–male competition and female mate choice on male CHC composition in the broad‐horned flour beetle Gnatocerus cornutus. We show that male–male competition exerts strong linear selection on both overall CHC abundance and body size in males, while female mate choice exerts a mixture of linear and nonlinear selection, targeting not just the overall amount of CHCs expressed but the relative abundance of specific hydrocarbons as well. We discuss the potential implications of this antagonistic selection with regard to male reproductive success.